Table Of ContentAbiotic Influences on Free-
Living Microbial Communities in
Hydrothermal Vent Ecosystems
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Citation Olins, Heather Craig. 2016. Abiotic Influences on Free-Living
Microbial Communities in Hydrothermal Vent Ecosystems. Doctoral
dissertation, Harvard University, Graduate School of Arts &
Sciences.
Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:33493269
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Abiotic!Influences!on!Free1Living!Microbial!Communities!!
in!Hydrothermal!Vent!Ecosystems!
!
!
a!dissertation!presented!
!
by!
!
Heather!Craig!Olins!
!
to!
!
The!Department!of!Organismic!and!Evolutionary!Biology!
!
in!partial!fulfillment!of!!the!requirements!
for!the!degree!of!
Doctor!of!Philosophy!
in!the!subject!of!
Biology!
!
Harvard!University!
Cambridge,!Massachusetts!
!
April!2016
!
!
!
©2016!I!!Heather!Craig!Olins!
all!rights!reserved!
! !
Dissertation!advisor:!Peter!R.!Girguis!! ! ! !!!!!!!!Heather!Craig!Olins!
!
!
Abiotic!Influences!on!Free1Living!Microbial!Communities!!
in!Hydrothermal!Vent!Ecosystems!
!
!
Abstract!
Hydrothermal! vent! ecosystems! are! defined! by! steep! thermal! and! chemical!
gradients.! Chemosynthetic!microorganisms! are! the! primary! producers! in! these! systems,!
utilizing!the!available!chemical!energy!to!support!substantial!animal!biomass.!The!variety!
of!chemical!substrates!provided!by!hydrothermal!fluid!and!surrounding!seawater!enables!a!
metabolically!diverse!community!of!microbes.!However,!our!understanding!of!how!abiotic!
factors!such!as!temperature,!geochemistry,!and!mineral!substrate!influence!the!activity!of!
these! microbes! is! limited.! The! overarching! goal! of! this! dissertation! is! to! examine! the!
influence! of! these! abiotic! factors! on! freeIliving! microbial! community! composition,!
structure,! and! function.! In! this! work! I! first! examined! the! influence! of! temperature! on!
primary! productivity! by! using! radio! isotopic! tracer! studies! to! measure! rates! of! carbon!
fixation!by!epiI!and!endolithic!microbial!communities! from!vent!chimney!sulfides.! I!show!
evidence! that! these! communities! fix!more! carbon!at! low! temperatures,! underscoring! the!
importance!of!low!temperature!habitats!in!these!environments!commonly!characterized!by!
high! temperature.! I! then! utilized! in# situ! RNA! preservation! to! examine! communityIwide!
microbial!activity!in!low!temperature!vent!fluids!throughout!a!vent!field.!These!data!show!
two!distinct!activity!profiles!that!crossIcut!canonical!habitat!descriptions,!and!highlight!the!
importance!of! the! intraIfield!waters!among! the!discrete!vents!as! regions!of!high!primary!
! iii!
productivity! bearing! similarity! in! microbial! activity! to! plumes! emanating! from! high!
temperature! chimneys.! Finally,! I! designed! novel! colonization! devices! to! examine! the!
influence! of! mineral! substrate! on! microbial! community! composition,! structure,! and!
succession.! Mineralogy! influenced! certain! taxa.! I! also! identified! potential! early! and! late!
successional!taxa.!The!combination!of!metabolic!rate!measurements,!metatranscriptomics,!
and! colonization! experiments! presented! here,! all! with! coIregistered! geochemistry,!
underscore! the! substantial! heterogeneity! of! these! systems! and! offer! insights! into! the!
relative!strengths!of!the!abiotic!forces!that!help!to!govern!these!ecosystems.!
! !
! !
! iv!
Assessing!the!Influence!of!Abiotic!Factors!on!!
Microbial!Communities!at!Hydrothermal!Vent!Ecosystems!
!
!
Table!of!Contents!
!
Acknowledgements! ! ! ! ! ! ! ! ! !!!!!!!vi!
!
Chapter!1! ! ! ! ! ! ! ! ! ! ! !!!!!!!!1!
Introduction!
!
Chapter!2!! ! ! ! ! ! ! ! ! ! ! !!!!!!13!
Assessing!the!influence!of!physical,!geochemical,!and!biological!factors!
on!anaerobic!microbial!primary!productivity!within!hydrothermal!vent!
chimneys!
!
Chapter!3! ! ! ! ! ! ! ! ! ! ! !!!!!!29!
CoIregistered!geochemistry!and!metatranscriptomics!reveal!an!
unexpected!distribution!of!microbial!activity!within!a!hydrothermal!vent!
field!
!
Chapter!4! ! ! ! ! ! ! ! ! ! ! !!!!!!81!
In#situ#mineral#colonization!samplers!reveal!patterns!in!microbial!
community!composition,!structure,!and!succession!
Chapter!5!! ! ! ! ! ! ! ! ! ! ! !!!116!
Conclusions!
!
Appendix!A!! ! ! ! ! ! ! ! ! ! !!!121!
Chapter!2!Supplemental!Material!
!
Appendix!B!! ! ! ! ! ! ! ! ! ! !!!130!
Chapter!3!Supplemental!Material!
!
Appendix!C!! ! ! ! ! ! ! ! ! ! !!!144!
Chapter!4!Supplemental!Material!
!
Appendix!D! ! ! ! ! ! ! ! ! ! !!!154!
SEM!imagery!of!ISMACS!minerals!
! v!
Acknowledgements!
!
! There!are!many!people!without!whom!I!would!have!given!up!on!myself!a!long!time!
ago.!My!advisor,!Peter!Girguis,! took!a!chance!on!me!I!a!student!who!knew!nothing!about!
microbiology!before!starting!in!his!lab.!I!am!incredibly!lucky!to!have!found!an!advisor!who!
genuinely! cares! for! the!people! in! his! lab,! and!whose!pep! talks! always! seem! to!make! the!
world!less!ominous!and!my!data!more!exciting.!Pete!has!helped!me!find!my!confidence!as!a!
scientist,! and! see! the! value! of! “wrench! science”! when! my! tendency! is! for! “duct! tape!
science”.! I!am! incredibly!grateful! for! the!value!he!always!placed!on!my! ideas,!and! for!his!
willingness!to!speak!openly!and!truly!listen!to!my!opinions!on!a!wide!variety!of!topics.!I!am!
also! very! grateful! to! my! committee! members! Andrew! Knoll! and! Colleen! Cavanaugh! for!
their!considerable!support!and!thoughtful,!detailed,!feedback!over!the!years.!!
The!Girguis!Lab!and!OEB!have!been!home!to!a!huge!number!of!incredible!scientists,!
colleagues,! and! friends! throughout! the! seven! years! I! have! been! a! part! of! them.! Despite!
“Girgoyles”!coming!and!going,!the!lab!has!always!had!a!wonderful!collegial!and!funIloving!
atmosphere,!and!has!always!felt!like!home.!I!don’t!know!what!I!would!have!done!without!
the! amazing! problem! solving,! morale! boosting,! and! general! awesomeness! of! Jennifer!
Delaney,! Stephanie!Hillsgrove,! and!Charles!Vidoudez.! PostIdocs!Mark!Nielsen! and!Daniel!
Rogers!were! important!mentors!who! shared! their! expertise! and! advice! generously,! and!
whose! presence! made! lab! more! fun.! Kiana! Frank! gave! me! a! personal! crash! course! in!
microbiology! and! taught! me! how! to! “cruise”! when! I! joined! the! lab,! for! which! I! will! be!
eternally! grateful.! Kiana,! Roxanne! Beinart,! and!Dipti! Nayak! have! each! taught!me! a! huge!
amount!of!nitty!gritty!science,!provided!more!support!than!they!will!ever!know,!and!most!
importantly! become! friends! who! feel! like! sisters.! I! am! grateful! for! the! wonderful!
! vi!
camaraderie! and! support! of! OEB! grad! students! Jon! Sanders,! Didem! Sarikaya,! Leonora!
Bittleston,! Shane! CampbellIStaton,! and! Ambika! Kamath,! you! have! inspired! me! to! be! a!
better!scientist!and!a!more!conscientious!person.!
I! have! benefited! from! the! knowledge! and! talents! of! a! long! list! of! coIauthors,!
collaborators,! and! scientists! who! gave! their! advice! freely:! Kiana! Frank,! Daniel! Rogers,!
Charles!Vidoudez,!Christina!Preston,!Bill!Ussler,!Chris!Scholin,!Amy!Gartman,!Xiaofei!Guan,!
Colleen!Hansel,! Anne!Pearson,!Deb!Kelley,! Frank! Stewart,! and!Aude!Picard.! Additionally,!
this!work!wold!have!been! impossible!without! the! talented! and! accommodating! crews!of!
the!R/V!Atlantis,!HOV!Alvin,!R/V!Western!Flyer,!and!ROV!Doc!Rickets.!
I! am! incredibly! lucky! to! have! a! wonderful! group! of! friends! and! family! beyond!
Harvard! who! have! supported! me! over! the! years.! Nina! Lanza,! Alison! Cristiello,! Rachel!
Fineman,!and!Kate!Piper!have!provided!inspiration,!perspective,!and!much!needed!laughs.!
My!extended!family!of!Donna,!Carl,!and!Jeff!Albro,!and!Leah!Sawyer!have!been!incredibly!
supportive! over! these! challenging! last! few! months,! stepping! up! whenever! I! needed!
anything.!My!siblings!Jake,!Shura,!and!Matt!Olins!have!all!inspired!me!in!different!ways,!and!
their! confidence! in!me! has! helped!me! have! confidence! in!myself.! My! husband! and! true!
partner!in!life!Donald!Albro!has!kept!me!laughing!throughout!everything,!and!knows!how!
to!take!care!of!me!when!I!don’t!know!I!need!care.!
Finally,! my! biggest! fans! over! the! decades,! my! parents! Elizabeth! CraigIOlins! and!
Andrew!Olins! have!made!me!who! I! am! today.!My! father! instilled! in!me! a! reverence! for!
knowledge,!reason,!and!education,!while!my!mother!inspired!my!passion!and!wonder!for!
the! natural!world.! I! do! not! have! the!words! to! adequately! express!my! gratitude! for! their!
unending!support!and!love.!
! vii!
Chapter!1!
Introduction!
! !
Why!study!microbial!communities!at!hydrothermal!vents?!!
The!vast!majority!of!life!on!Earth!depends!on!sunlight,!either!directly!or!indirectly,!
for! its! energy.!Even! in! the!dark!deep! sea,!most! organisms!are!dependent!on! energy! that!
drifts!down!from!the!sunlit!surface!water!in!the!form!of!dead!or!decaying!organic!matter.!
Hydrothermal!vents,!on!the!other!hand,!represent!an!ecosystem!that!relies!on!a!completely!
different!energy!source!I!chemicals!from!within!the!Earth!I!and!microbes!that!can!perform!
chemosynthesis!to!exploit!that!energy.!While!many!vent!organisms!are!still!dependent!on!
oxygen! initially! generated! through! photosynthesis,! this! chemical! energy! source!
distinguishes! deep! sea! hydrothermal! vents! as! unique.! Ultimately,! our! understanding! of!
biology!is!incomplete!without!understanding!such!a!distinct!system!of!ecosystem!support.!
The!microbial! communities! investigated! in! this! dissertation! are! relevant! far! beyond! the!
deep!sea,!and!are!important!for!a!diverse!set!of!reasons!including!a!better!understanding!of!
global! biogeochemical! cycles,! the! global! search! for! valuable! mineral! and! biological!
resources,! exploration! of! the! origin! of! life! on! Earth,! and! even! the! search! for! life! beyond!
Earth.! !
As! awareness! of! global! climate! change! grows,! so! does! the! importance! of!
understanding! Earth’s! biogeochemical! cycles.! A! volume! of!water! equal! to! that! of! Earth’s!
global! ocean! cycles! through! the! midIocean! ridge! system! every! 70,000I200,000! years!
(Wheat! et#al.,! 2003;! Johnson! and! Pruis,! 2003).! As! such,! hydrothermal! vents! (where! this!
fluid! reIenters! the! ocean)! are! a! global! phenomenon! and! exert! influence! over! certain!
aspects!of!global!ocean!chemistry.!In!particular,!the!global!iron!cycle!is!strongly!influenced!
by! mid! ocean! ridge! hydrothermal! venting! from! which! iron! is! transported! thousands! of!
kilometers! and! accounts! for! a! substantial! fraction! of! total! dissolved! iron! (Resing! et# al.,!
! 2
